Contributions of the Ventral Striatum to Conscious Perception: An Intracranial EEG Study of the Attentional Blink

Abstract

The brain is limited in its capacity to consciously process information, necessitating gating of information. While conscious perception is robustly associated with sustained, recurrent interactions between widespread cortical regions, subcortical regions, including the striatum, influence cortical activity. Here, we examined whether the ventral striatum, given its ability to modulate cortical information flow, contributes to conscious perception. Using intracranial EEG, we recorded ventral striatum activity while 7 patients performed an attentional blink task in which they had to detect two targets (T1 and T2) in a stream of distractors. Typically, when T2 follows T1 within 100-500 ms, it is often not perceived (i.e., the attentional blink). We found that conscious T2 perception was influenced and signaled by ventral striatal activity. Specifically, the failure to perceive T2 was foreshadowed by a T1-induced increase in α and low β oscillatory activity as early as 80 ms after T1, indicating that the attentional blink to T2 may be due to very early T1-driven attentional capture. Moreover, only consciously perceived targets were associated with an increase in θ activity between 200 and 400 ms. These unique findings shed new light on the mechanisms that give rise to the attentional blink by revealing that conscious target perception may be determined by T1 processing at a much earlier processing stage than traditionally believed. More generally, they indicate that ventral striatum activity may contribute to conscious perception, presumably by gating cortical information flow.

Significance statement: What determines whether we become aware of a piece of information or not? Conscious access has been robustly associated with activity within a distributed network of cortical regions. Using intracranial electrophysiological recordings during an attentional blink task, we tested the idea that the ventral striatum, because of its ability to modulate cortical information flow, may contribute to conscious perception. We find that conscious perception is influenced and signaled by ventral striatal activity. Short-latency (80-140 ms) striatal responses to a first target determined conscious perception of a second target. Moreover, conscious perception of the second target was signaled by longer-latency (200-400 ms) striatal activity. These results suggest that the ventral striatum may be part of a subcortical network that influences conscious experience.

Keywords: attentional blink; consciousness; intracranial EEG; oscillations; perception; striatum.

Figure 1.

A, Schematic illustration of deep-brain electrodes in the ventral striatum. Red represents the core of the nucleus accumbens (NAc). Adapted with permission from Figee et al. (2013). B, The AB task. Subjects had to detect two targets (T1 and T2; two numbers) in a rapid stream of distractor stimuli. Shown is an example of a short T1–T2 interval trial.

Figure 2.

AB task performance. Percentage T1 accuracy (left) and percentage T2 accurate given T1 correct (T2/T1) (right) are shown separately for short (200 ms) and long (800 ms) T1–T2 interval trials, for each patient (lines) and at the group level (bars). As shown, a robust AB was observed as reflected by lower T2/T1 accuracy in short interval compared with long interval trials. Error bars indicate SEM.

Figure 3.

The AB is predicted by, and reflected in, ventral striatal activity. Shown are intracranial EEG data from the left and right ventral striatum. A, Time-frequency representations show z values reflecting the strength of differences in striatal activity between T2-seen and T2-unseen short-interval trials. Time-frequency windows where the difference reached significance are highlighted in black. Average power (in dB) within these significant windows is shown in B separately for T2-unseen and T2-seen trials. The AB was associated with an early difference in T1-induced α and low β activity (8–16) between 80 and 140 ms after T1 in the left ventral striatum. Moreover, conscious T2 perception was associated with an increase in θ activity (4–8 Hz) between 215 and 400 ms after T2 in the left ventral striatum and between 150 and 280 ms after T2 in the right ventral striatum. Finally, in the right ventral striatum, perceived T2s elicited greater activity in the β-band (15–30 Hz) activity between 210 and 260 ms after T2 than T2s that went undetected. Thus, the AB to T2 was foreshadowed by a short-latency response to T1 in the left ventral striatum, and conscious T2 perception was signaled by longer-latency ventral striatal activity in the θ and β bands.

Figure 4.

The failure to perceive T2 is foreshadowed by early (80–140 ms) T1 processing in the ventral striatum, and conscious T2 target perception is associated with later (200–400 ms) ventral striatal activity. Shown are intracranial EEG data from the left (left figures) and right (right figures) ventral striatum. Time-frequency representations show oscillatory activity induced by T1 and T2 A, Short-interval T2-unseen B, short-interval T2-seen, and C, long-interval T2-seen trials. In trials in which T2 was not seen, T1 induced a strong increase in α and low β oscillatory activity (8–16) between 80 and 140 ms after T1 in the left ventral striatum. Moreover, in the left ventral striatum, when T2 was consciously perceived, an increase in θ oscillatory activity (4–8 Hz) was observed 215–400 ms after each target onset. However, when only T1 was seen, only the first increase in θ activity was present. Moreover, the second increase in θ activity is shifted in time with the presentation of T2 in long-interval trials, confirming that it is related to conscious perception of T2. Thus, only consciously perceived targets were signaled by θ oscillatory activity between 200 and 400 ms, in particular, in the left ventral striatum. Finally, conscious T2 perception was associated with a transient increase in β-band activity (15–30 Hz) in the right ventral striatum 210–260 ms after T2.